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Parasites & vectors2018; 11(1); 61; doi: 10.1186/s13071-018-2638-6

Cyathostomine egg reappearance period following ivermectin treatment in a cohort of UK Thoroughbreds.

Abstract: In spite of the emergence of populations of drug-resistant cyathostomines worldwide, little is known of parasite species responsible for 'early egg shedding' in cohorts of horses subjected to treatment with widely used anthelmintics, e.g. ivermectin (IVM). In this study, we determined the cyathostomine egg reappearance period (ERP) after IVM treatment in a cohort of yearlings from a large Thoroughbred (TB) stud farm in the United Kingdom, and identified species of cyathostomines with reduced ERP using a combination of fundamental parasitology techniques coupled with advanced molecular tools. Individual faecal samples were collected from TB yearlings with cyathostomine infection prior to IVM treatment, as well as at 14, 21, 28, 35, 42 and 49 days post-treatment. Faecal egg counts (FEC) were performed for each individual sample for determination of ERPs. In addition, individual larval cultures were performed and representative numbers of third-stage larvae (L3s) harvested from each culture were subjected to molecular species identification via PCR-Reverse Line Blot (RLB). Prior to IVM treatment, 11 cyathostomine species were detected in faecal samples from TB horses enrolled in this study, i.e. Cyathostomum catinatum, Cylicostephanus longibursatus, Cylicostephanus goldi, Cylicocyclus nassatus, Cylicostephanus calicatus, Cyathostomum pateratum, Cylicocyclus radiatus, Paraposteriostomum mettami, Coronocyclus labratus, Cylicocyclus insigne and Cylicocyclus radiatus variant A. Of these, eggs of Cya. catinatum, Cys. longibursatus, Cyc. nassatus and Cyc. radiatus could be detected at 28 days post-treatment, while from day 42 onwards, cyathostomine species composition reflected data obtained pre-IVM treatment, with the exception of eggs of Cor. labratus and Cyc. insigne which could no longer be detected post-IVM administration. This study provides valuable data on the occurrence of IVM-resistance in cyathostomines in the UK. Nevertheless, further investigations are needed to shed light on the prevalence and incidence of drug-resistance in this country, as well as other areas of the world where equine trade is substantial.
Publication Date: 2018-01-25 PubMed ID: 29370872PubMed Central: PMC5785887DOI: 10.1186/s13071-018-2638-6Google Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The study investigates drug-resistant cyathostomines or small strongyles, a common equine internal parasite. The researchers observed the time it took for cyathostomine eggs to reappear in horse feces after treatment with ivermectin, an antiparasitic medication. The team identified which species of cyathostomines developed resistance to the drug.

Objective of the Study

  • The study was designed to understand the emergence of drug-resistant cyathostomines in horses. Cyathostomines are a group of parasitic worms that infect horses and are currently exhibiting resistance to commonly used antiparasitic drugs such as ivermectin.
  • The researchers aimed to determine the egg reappearance period (ERP), or the time it takes for cyathostomine eggs to reappear in the feces of horses after being treated with ivermectin. This would allow them to identify the species of cyathostomines displaying reduced ERP, implying resistance to the drug.

Methodology

  • Fecal samples were collected from Thoroughbred yearling horses with cyathostomine infection before and after treatment with ivermectin. The collection took place at different intervals: 14, 21, 28, 35, 42, and 49 days post-treatment. Researchers conducted faecal egg counts (FEC) for each sample to determine ERPs.
  • In addition, larval cultures for each individual sample were analyzed. Select numbers of third-stage larvae from each culture were used for molecular species identification via PCR-Reverse Line Blot (RLB).

Findings

  • Before treatment, 11 cyathostomine species were identified from the fecal samples of the studied horses.
  • Four species appeared to show resistance to medication, as their eggs could be detected 28 days after treatment.
  • By 42 days post-treatment, the cyathostomine species composition mirrored the pre-treatment data, except for two species whose eggs could no longer be detected after ivermectin administration, suggesting that they were susceptible to the drug treatment.

Conclusions

  • This study provides critical information on the existence of ivermectin-resistant cyathostomines in the UK.
  • However, more research is needed to understand the prevalence and incidence of drug resistance in the country and other regions of the world where horse trade is substantial.

Cite This Article

APA
Molena RA, Peachey LE, Di Cesare A, Traversa D, Cantacessi C. (2018). Cyathostomine egg reappearance period following ivermectin treatment in a cohort of UK Thoroughbreds. Parasit Vectors, 11(1), 61. https://doi.org/10.1186/s13071-018-2638-6

Publication

ISSN: 1756-3305
NlmUniqueID: 101462774
Country: England
Language: English
Volume: 11
Issue: 1
Pages: 61
PII: 61

Researcher Affiliations

Molena, Rebecca A
  • Department of Veterinary Medicine, University of Cambridge, Cambridge, UK.
Peachey, Laura E
  • Department of Veterinary Medicine, University of Cambridge, Cambridge, UK.
Di Cesare, Angela
  • Faculty of Veterinary Medicine, University of Teramo, Località Piano d'Accio, Teramo, Italy.
Traversa, Donato
  • Faculty of Veterinary Medicine, University of Teramo, Località Piano d'Accio, Teramo, Italy.
Cantacessi, Cinzia
  • Department of Veterinary Medicine, University of Cambridge, Cambridge, UK. cc779@cam.ac.uk.

MeSH Terms

  • Animals
  • Anthelmintics / administration & dosage
  • Drug Resistance
  • Feces / parasitology
  • Horse Diseases / drug therapy
  • Horse Diseases / parasitology
  • Horses
  • Ivermectin / administration & dosage
  • Parasite Egg Count
  • Polymerase Chain Reaction
  • Recurrence
  • Strongylida Infections / drug therapy
  • Strongylida Infections / parasitology
  • Strongylida Infections / veterinary
  • Strongyloidea / classification
  • Strongyloidea / genetics
  • Strongyloidea / isolation & purification
  • Time Factors
  • United Kingdom

Conflict of Interest Statement

ETHICS APPROVAL AND CONSENT TO PARTICIPATE: This study was approved and carried out in strict accordance and compliance with the guidelines of the Institutional Ethical Review Committee, Department of Veterinary Medicine, University of Cambridge, UK (Research Project No. CR190). Written informed consent was obtained from the stud farm from which study samples were collected. CONSENT FOR PUBLICATION: Not applicable. COMPETING INTERESTS: The authors declare that they have no competing interests. PUBLISHER’S NOTE: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

This article includes 84 references
  1. Mfitilodze MW, Hutchinson GW. Prevalence and abundance of equine strongyles (Nematoda: Strongyloidea) in tropical Australia.. J Parasitol 1990 Aug;76(4):487-94.
    doi: 10.2307/3282826pubmed: 2380857google scholar: lookup
  2. Collobert-Laugier C, Hoste H, Sevin C, Dorchies P. Prevalence, abundance and site distribution of equine small strongyles in Normandy, France.. Vet Parasitol 2002 Dec 11;110(1-2):77-83.
    doi: 10.1016/S0304-4017(02)00328-Xpubmed: 12446091google scholar: lookup
  3. Hinney B, Wirtherle NC, Kyule M, Miethe N, Zessin KH, Clausen PH. Prevalence of helminths in horses in the state of Brandenburg, Germany.. Parasitol Res 2011 May;108(5):1083-91.
    doi: 10.1007/s00436-011-2362-zpubmed: 21472400google scholar: lookup
  4. Morariu S, Mederle N, Badea C, Dărăbuş G, Ferrari N, Genchi C. The prevalence, abundance and distribution of cyathostomins (small stongyles) in horses from Western Romania.. Vet Parasitol 2016 Jun 15;223:205-9.
    pubmed: 27198801doi: 10.1016/j.vetpar.2016.04.021google scholar: lookup
  5. Lichtenfels JR, Kharchenko VA, Krecek RC, Gibbons LM. An annotated checklist by genus and species of 93 species level names for 51 recognized species of small strongyles (Nematoda: Strongyloidea: Cyathostominea) of horses, asses and zebras of the world.. Vet Parasitol 1998 Sep;79(1):65-79.
    doi: 10.1016/S0304-4017(98)00149-6pubmed: 9777726google scholar: lookup
  6. Lichtenfels JR, Gibbons LM, Krecek RC. Recommended terminology and advances in the systematics of the Cyathostominea (Nematoda: Strongyloidea) of horses.. Vet Parasitol 2002 Aug 22;107(4):337-42.
    doi: 10.1016/S0304-4017(02)00167-Xpubmed: 12163244google scholar: lookup
  7. Matthee S, Krecek RC, Gibbons LM. Cylicocyclus asini n. sp. (Nematoda: Cyathostominae) from donkeys Equus asinus in South Africa.. Syst Parasitol 2002 Jan;51(1):29-35.
    pubmed: 11721193doi: 10.1023/a:1012989810087google scholar: lookup
  8. Ogbourne CP. Observations on the free-living stages of strongylid nematodes of the horse.. Parasitology 1972 Jun;64(3):461-77.
    doi: 10.1017/S0031182000045534pubmed: 5039342google scholar: lookup
  9. Chapman MR, Kearney MT, Klei TR. An experimental evaluation of methods used to enumerate mucosal cyathostome larvae in ponies.. Vet Parasitol 1999 Oct 1;86(3):191-202.
    doi: 10.1016/S0304-4017(99)00144-2pubmed: 10511101google scholar: lookup
  10. Gibson TE. The effect of repeated anthelmintic treatment with phenothiazine on the faecal egg counts of housed horses, with some observations on the life cycle of Trichonema spp. in the horse.. J Helminthol 1953;27:29–40.
    doi: 10.1017/S0022149X00023488google scholar: lookup
  11. Corning S. Equine cyathostomins: a review of biology, clinical significance and therapy.. Parasit Vectors 2009 Sep 25;2 Suppl 2(Suppl 2):S1.
    doi: 10.1186/1756-3305-2-S2-S1pmc: PMC2751837pubmed: 19778462google scholar: lookup
  12. Love S, Duncan JL. The development of naturally acquired cyathostome infection in ponies.. Vet Parasitol 1992 Sep;44(1-2):127-42.
    doi: 10.1016/0304-4017(92)90151-Xpubmed: 1441184google scholar: lookup
  13. Love S, Murphy D, Mellor D. Pathogenicity of cyathostome infection.. Vet Parasitol 1999 Aug 31;85(2-3):113-21; discussion 121-2, 215-25.
    doi: 10.1016/S0304-4017(99)00092-8pubmed: 10485358google scholar: lookup
  14. Kornaś S, Cabaret J, Skalska M, Nowosad B. Horse infection with intestinal helminths in relation to age, sex, access to grass and farm system.. Vet Parasitol 2010 Dec 15;174(3-4):285-91.
    doi: 10.1016/j.vetpar.2010.09.007pubmed: 20933334google scholar: lookup
  15. Mirck MH. [Cyathostominosis: a form of severe strongylidosis (author's transl)].. Tijdschr Diergeneeskd 1977 Aug 1;102(15):876-8.
    pubmed: 560729
  16. Ogbourne C. Pathogenesis of cyathostome Trichonema infections of the horse. A review.. Farnham Royal, Slough: Commonwealth Agricultural Bureau; 1978. p. 25.
  17. Giles CJ, Urquhart KA, Longstaffe JA. Larval cyathostomiasis (immature trichonema-induced enteropathy): a report of 15 clinical cases.. Equine Vet J 1985 May;17(3):196-201.
  18. Uhlinger C. Effects of three anthelmintic schedules on the incidence of colic in horses.. Equine Vet J 1990 Jul;22(4):251-4.
  19. Mair TS, Pearson GR. Multifocal non-strangulating intestinal infarction associated with larval cyathostomiasis in a pony.. Equine Vet J 1995 Mar;27(2):154-5.
  20. Mair TS, Sutton DG, Love S. Caecocaecal and caecocolic intussusceptions associated with larval cyathostomosis in four young horses.. Equine Vet J Suppl 2000 Jun;(32):77-80.
  21. Khan M, Roohi N, Rana M. Strongylosis in equines: a review.. J Anim Plant Sci 2015;25:1–9.
  22. Bland S. Equine colic: a review of the equine hindgut and colic.. Vet Sci Dev 2016;6223:48–51.
  23. Debeffe L, McLoughlin PD, Medill SA, Stewart K, Andres D, Shury T, Wagner B, Jenkins E, Gilleard JS, Poissant J. Negative covariance between parasite load and body condition in a population of feral horses.. Parasitology 2016 Jul;143(8):983-97.
    doi: 10.1017/S0031182016000408pubmed: 27046508google scholar: lookup
  24. BAKER NF, DOUGLAS JR. Critical trials with thiabendazole as an anthelmintic in the gastrointestinal tract of cattle and sheep.. Am J Vet Res 1962 Nov;23:1219-23.
    pubmed: 13969162
  25. BELL RR, GALVIN TJ, TURK RD. Anthelmintics for ruminants. VI. Thiabendazole.. Am J Vet Res 1962 Mar;23:195-200.
    pubmed: 13866839
  26. Lyons ET, Drudge JH, Tolliver SC, Breukink HJ. Critical test of three salts of pyrantel against internal parasites of the horse.. Am J Vet Res 1974 Dec;35(12):1515-22.
    pubmed: 4279571
  27. Slocombe JO, Smart J. Evaluation of pyrantel pamoate against strongyles in horses.. Can Vet J 1975 Oct;16(10):310-2.
    pmc: PMC1697063pubmed: 1192342
  28. Campbell WC, Fisher MH, Stapley EO, Albers-Schönberg G, Jacob TA. Ivermectin: a potent new antiparasitic agent.. Science 1983 Aug 26;221(4613):823-8.
    doi: 10.1126/science.6308762pubmed: 6308762google scholar: lookup
  29. Slocombe JO, Cote JF. Effectiveness of ivermectin paste for removal of nematodes in the horse.. Can Vet J 1984 Oct;25(10):386-8.
    pmc: PMC1790654pubmed: 17422461
  30. Lyons ET, Tolliver SC, Drudge JH, Granstrom DE, Collins SS, Stamper S. Critical and controlled tests of activity of moxidectin (CL 301,423) against natural infections of internal parasites of equids.. Vet Parasitol 1992 Mar;41(3-4):255-84.
    doi: 10.1016/0304-4017(92)90086-Opubmed: 1502789google scholar: lookup
  31. Matthews JB. An update on cyathostomins: anthelmintic resistance and worm control.. Equine Vet Educ 2008;20:552–560.
    doi: 10.2746/095777308X363912google scholar: lookup
  32. Stratford CH, McGorum BC, Pickles KJ, Matthews JB. An update on cyathostomins: anthelmintic resistance and diagnostic tools.. Equine Vet J Suppl 2011 Aug;(39):133-9.
  33. Peregrine AS, Molento MB, Kaplan RM, Nielsen MK. Anthelmintic resistance in important parasites of horses: does it really matter?. Vet Parasitol 2014 Mar 17;201(1-2):1-8.
    doi: 10.1016/j.vetpar.2014.01.004pubmed: 24485565google scholar: lookup
  34. Tzelos T, Matthews JB. Anthelmintic resistance in equine helminths and mitigating its effects.. In Pract 2016;38:489–499.
    doi: 10.1136/inp.i5287google scholar: lookup
  35. Kaplan RM, Klei TR, Lyons ET, Lester G, Courtney CH, French DD, Tolliver SC, Vidyashankar AN, Zhao Y. Prevalence of anthelmintic resistant cyathostomes on horse farms.. J Am Vet Med Assoc 2004 Sep 15;225(6):903-10.
    doi: 10.2460/javma.2004.225.903pubmed: 15485051google scholar: lookup
  36. Lind EO, Rautalinko E, Uggla A, Waller PJ, Morrison DA, Höglund J. Parasite control practices on Swedish horse farms.. Acta Vet Scand 2007 Sep 26;49(1):25.
    doi: 10.1186/1751-0147-49-25pmc: PMC2093939pubmed: 17897438google scholar: lookup
  37. Traversa D, Klei TR, Iorio R, Paoletti B, Lia RP, Otranto D, Sparagano OA, Giangaspero A. Occurrence of anthelmintic resistant equine cyathostome populations in central and southern Italy.. Prev Vet Med 2007 Dec 14;82(3-4):314-20.
  38. Traversa D, von Samson-Himmelstjerna G, Demeler J, Milillo P, Schürmann S, Barnes H, Otranto D, Perrucci S, di Regalbono AF, Beraldo P, Boeckh A, Cobb R. Anthelmintic resistance in cyathostomin populations from horse yards in Italy, United Kingdom and Germany.. Parasit Vectors 2009 Sep 25;2 Suppl 2(Suppl 2):S2.
    pmc: PMC2751838pubmed: 19778463doi: 10.1186/1756-3305-2-s2-s2google scholar: lookup
  39. Traversa D, Castagna G, von Samson-Himmelstjerna G, Meloni S, Bartolini R, Geurden T, Pearce MC, Woringer E, Besognet B, Milillo P, D'Espois M. Efficacy of major anthelmintics against horse cyathostomins in France.. Vet Parasitol 2012 Sep 10;188(3-4):294-300.
    doi: 10.1016/j.vetpar.2012.03.048pubmed: 22538094google scholar: lookup
  40. Lester HE, Spanton J, Stratford CH, Bartley DJ, Morgan ER, Hodgkinson JE, Coumbe K, Mair T, Swan B, Lemon G, Cookson R, Matthews JB. Anthelmintic efficacy against cyathostomins in horses in Southern England.. Vet Parasitol 2013 Oct 18;197(1-2):189-96.
    doi: 10.1016/j.vetpar.2013.06.009pubmed: 23830687google scholar: lookup
  41. Lyons ET, Tolliver SC, Drudge JH, Collins SS, Swerczek TW. Continuance of studies on Population S benzimidazole-resistant small strongyles in a Shetland pony herd in Kentucky: effect of pyrantel pamoate (1992-1999).. Vet Parasitol 2001 Jan 20;94(4):247-56.
    doi: 10.1016/S0304-4017(00)00382-4pubmed: 11137272google scholar: lookup
  42. Nielsen M, Mittel L, Grice A, Erskine M, Graves E, Vaala W. AAEP Parasite Control Guidelines.. 2013.
  43. Stratford CH, Lester HE, Pickles KJ, McGorum BC, Matthews JB. An investigation of anthelmintic efficacy against strongyles on equine yards in Scotland.. Equine Vet J 2014 Jan;46(1):17-24.
    doi: 10.1111/evj.12079pubmed: 23662803google scholar: lookup
  44. Epe C, Kaminsky R. New advancement in anthelmintic drugs in veterinary medicine.. Trends Parasitol 2013 Mar;29(3):129-34.
    doi: 10.1016/j.pt.2013.01.001pubmed: 23376212google scholar: lookup
  45. Relf VE, Morgan ER, Hodgkinson JE, Matthews JB. A questionnaire study on parasite control practices on UK breeding Thoroughbred studs.. Equine Vet J 2012 Jul;44(4):466-71.
  46. Nielsen MK, Monrad J, Olsen SN. Prescription-only anthelmintics--a questionnaire survey of strategies for surveillance and control of equine strongyles in Denmark.. Vet Parasitol 2006 Jan 15;135(1):47-55.
    doi: 10.1016/j.vetpar.2005.10.020pubmed: 16309841google scholar: lookup
  47. Molento MB, Antunes J, Bentes RN, Coles GC. Anthelmintic resistant nematodes in Brazilian horses.. Vet Rec 2008 Mar 22;162(12):384-5.
    doi: 10.1136/vr.162.12.384pubmed: 18359933google scholar: lookup
  48. Milillo P, Boeckh A, Cobb R, Otranto D, Lia RP, Perrucci S, di Regalbono AF, Beraldo P, von Samson-Himmelstjerna G, Demeler J, Bartolini R, Traversa D. Faecal Cyathostomin Egg Count distribution and efficacy of anthelmintics against cyathostomins in Italy: a matter of geography?. Parasit Vectors 2009 Sep 25;2 Suppl 2(Suppl 2):S4.
    pmc: PMC2751840pubmed: 19778465doi: 10.1186/1756-3305-2-s2-s4google scholar: lookup
  49. Trawford AF, Burden FA, Hodgkinson J. Suspected moxidectin resistance in cyathostomes in two donkey herds at the donkey sanctuary, UK.. Christchurch: Proceedings of the 20th International Conference of the World Association for Advancement in Veterinary Parasitology; 2005.
  50. Näreaho A, Vainio K, Oksanen A. Impaired efficacy of ivermectin against Parascaris equorum, and both ivermectin and pyrantel against strongyle infections in trotter foals in Finland.. Vet Parasitol 2011 Dec 15;182(2-4):372-7.
    doi: 10.1016/j.vetpar.2011.05.045pubmed: 21689886google scholar: lookup
  51. Canever RJ, Braga PR, Boeckh A, Grycajuck M, Bier D, Molento MB. Lack of Cyathostomin sp. reduction after anthelmintic treatment in horses in Brazil.. Vet Parasitol 2013 May 1;194(1):35-9.
    doi: 10.1016/j.vetpar.2012.12.020pubmed: 23318166google scholar: lookup
  52. Relf VE, Lester HE, Morgan ER, Hodgkinson JE, Matthews JB. Anthelmintic efficacy on UK Thoroughbred stud farms.. Int J Parasitol 2014 Jul;44(8):507-14.
    doi: 10.1016/j.ijpara.2014.03.006pubmed: 24746779google scholar: lookup
  53. Tzelos T, Barbeito JS, Nielsen MK, Morgan ER, Hodgkinson JE, Matthews JB. Strongyle egg reappearance period after moxidectin treatment and its relationship with management factors in UK equine populations.. Vet Parasitol 2017 Apr 15;237:70-76.
    doi: 10.1016/j.vetpar.2017.02.018pubmed: 28249767google scholar: lookup
  54. Lyons ET, Tolliver SC, Collins SS. Probable reason why small strongyle EPG counts are returning "early" after ivermectin treatment of horses on a farm in Central Kentucky.. Parasitol Res 2009 Feb;104(3):569-74.
    doi: 10.1007/s00436-008-1231-xpubmed: 18931857google scholar: lookup
  55. van Doorn DC, Ploeger HW, Eysker M, Geurden T, Wagenaar JA, Kooyman FN. Cylicocyclus species predominate during shortened egg reappearance period in horses after treatment with ivermectin and moxidectin.. Vet Parasitol 2014 Dec 15;206(3-4):246-52.
    doi: 10.1016/j.vetpar.2014.10.004pubmed: 25458565google scholar: lookup
  56. Kooyman FN, van Doorn DC, Geurden T, Wagenaar JA. Semi-quantitative differentiation of cyathostomin larval cultures by reverse line blot.. Vet Parasitol 2016 Jan 30;216:59-65.
    doi: 10.1016/j.vetpar.2015.12.009pubmed: 26801596google scholar: lookup
  57. Ionita M, Howe DK, Lyons ET, Tolliver SC, Kaplan RM, Mitrea IL, Yeargan M. Use of a reverse line blot assay to survey small strongyle (Strongylida: Cyathostominae) populations in horses before and after treatment with ivermectin.. Vet Parasitol 2010 Mar 25;168(3-4):332-7.
    doi: 10.1016/j.vetpar.2009.11.021pubmed: 20045254google scholar: lookup
  58. Bellaw JL, Krebs K, Reinemeyer CR, Norris JK, Scare JA, Pagano S, Nielsen MK. Anthelmintic therapy of equine cyathostomin nematodes - larvicidal efficacy, egg reappearance period, and drug resistance.. Int J Parasitol 2018 Feb;48(2):97-105.
    pubmed: 29050919doi: 10.1016/j.ijpara.2017.08.009google scholar: lookup
  59. Bartley DJ, Donnan AA, Jackson E, Sargison N, Mitchell GB, Jackson F. A small scale survey of ivermectin resistance in sheep nematodes using the faecal egg count reduction test on samples collected from Scottish sheep.. Vet Parasitol 2006 Apr 15;137(1-2):112-8.
    doi: 10.1016/j.vetpar.2005.12.014pubmed: 16426761google scholar: lookup
  60. Rehbein S, Lindner T, Visser M, Winter R. Evaluation of a double centrifugation technique for the detection of Anoplocephala eggs in horse faeces.. J Helminthol 2011 Dec;85(4):409-14.
    doi: 10.1017/S0022149X10000751pubmed: 21138608google scholar: lookup
  61. Coles GC, Bauer C, Borgsteede FH, Geerts S, Klei TR, Taylor MA, Waller PJ. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) methods for the detection of anthelmintic resistance in nematodes of veterinary importance.. Vet Parasitol 1992 Sep;44(1-2):35-44.
    pubmed: 1441190doi: 10.1016/0304-4017(92)90141-ugoogle scholar: lookup
  62. Vidyashankar AN, Kaplan RM, Chan S. Statistical approach to measure the efficacy of anthelmintic treatment on horse farms.. Parasitology 2007 Dec;134(Pt.14):2027-39.
    doi: 10.1017/S003118200700340Xpubmed: 17714603google scholar: lookup
  63. Kaplan RM, Nielsen MK. An evidence-based approach to equine parasite control: it ain't the 60s anymore.. Equine Vet Educ 2010;22:306–316.
  64. Larsen ML, Ritz C, Petersen SL, Nielsen MK. Determination of ivermectin efficacy against cyathostomins and Parascaris equorum on horse farms using selective therapy.. Vet J 2011 Apr;188(1):44-7.
    doi: 10.1016/j.tvjl.2010.03.009pubmed: 20385508google scholar: lookup
  65. van Doorn DC, Kooyman FN, Eysker M, Hodgkinson JE, Wagenaar JA, Ploeger HW. In vitro selection and differentiation of ivermectin resistant cyathostomin larvae.. Vet Parasitol 2010 Dec 15;174(3-4):292-9.
    doi: 10.1016/j.vetpar.2010.08.021pubmed: 20850222google scholar: lookup
  66. Traversa D, Iorio R, Klei TR, Kharchenko VA, Gawor J, Otranto D, Sparagano OA. New method for simultaneous species-specific identification of equine strongyles (nematoda, strongylida) by reverse line blot hybridization.. J Clin Microbiol 2007 Sep;45(9):2937-42.
    doi: 10.1128/JCM.00714-07pmc: PMC2045237pubmed: 17626168google scholar: lookup
  67. Cwiklinski K, Kooyman FN, Van Doorn DC, Matthews JB, Hodgkinson JE. New insights into sequence variation in the IGS region of 21 cyathostomin species and the implication for molecular identification.. Parasitology 2012 Jul;139(8):1063-73.
    doi: 10.1017/S0031182012000467pubmed: 22717256google scholar: lookup
  68. Piché CA, Kennedy MJ, Herbers HA, Newcomb KM. Comparison of ivermectin, oxibendazole, and pyrantel pamoate in suppressing fecal egg output in horses.. Can Vet J 1991 Feb;32(2):104-7.
    pmc: PMC1480944pubmed: 17423731
  69. Demeulenaere D, Vercruysse J, Dorny P, Claerebout E. Comparative studies of ivermectin and moxidectin in the control of naturally acquired cyathostome infections in horses.. Vet Rec 1997 Oct 11;141(15):383-6.
    doi: 10.1136/vr.141.15.383pubmed: 9364706google scholar: lookup
  70. von Samson-Himmelstjerna G, Fritzen B, Demeler J, Schürmann S, Rohn K, Schnieder T, Epe C. Cases of reduced cyathostomin egg-reappearance period and failure of Parascaris equorum egg count reduction following ivermectin treatment as well as survey on pyrantel efficacy on German horse farms.. Vet Parasitol 2007 Mar 15;144(1-2):74-80.
    doi: 10.1016/j.vetpar.2006.09.036pubmed: 17112667google scholar: lookup
  71. Geurden T, van Doorn D, Claerebout E, Kooyman F, De Keersmaecker S, Vercruysse J, Besognet B, Vanimisetti B, di Regalbono AF, Beraldo P, Di Cesare A, Traversa D. Decreased strongyle egg re-appearance period after treatment with ivermectin and moxidectin in horses in Belgium, Italy and The Netherlands.. Vet Parasitol 2014 Aug 29;204(3-4):291-6.
    pubmed: 24880643doi: 10.1016/j.vetpar.2014.04.013google scholar: lookup
  72. van Wyk JA. Refugia--overlooked as perhaps the most potent factor concerning the development of anthelmintic resistance.. Onderstepoort J Vet Res 2001 Mar;68(1):55-67.
    pubmed: 11403431
  73. Matthee S, Krecek RC, Milne SA, Boshoff M, Guthrie AJ. Impact of management interventions on helminth levels, and body and blood measurements in working donkeys in South Africa.. Vet Parasitol 2002 Jul 29;107(1-2):103-13.
    doi: 10.1016/S0304-4017(02)00113-9pubmed: 12072218google scholar: lookup
  74. Nielsen MK. Sustainable equine parasite control: perspectives and research needs.. Vet Parasitol 2012 Apr 19;185(1):32-44.
    doi: 10.1016/j.vetpar.2011.10.012pubmed: 22055611google scholar: lookup
  75. Lester HE, Bartley DJ, Morgan ER, Hodgkinson JE, Stratford CH, Matthews JB. A cost comparison of faecal egg count-directed anthelmintic delivery versus interval programme treatments in horses.. Vet Rec 2013 Oct 19;173(15):371.
    doi: 10.1136/vr.101804pubmed: 24068698google scholar: lookup
  76. Kooyman FN, van Doorn DC, Geurden T, Mughini-Gras L, Ploeger HW, Wagenaar JA. Species composition of larvae cultured after anthelmintic treatment indicates reduced moxidectin susceptibility of immature Cylicocyclus species in horses.. Vet Parasitol 2016 Aug 30;227:77-84.
    doi: 10.1016/j.vetpar.2016.07.029pubmed: 27523942google scholar: lookup
  77. Blackhall WJ, Pouliot JF, Prichard RK, Beech RN. Haemonchus contortus: selection at a glutamate-gated chloride channel gene in ivermectin- and moxidectin-selected strains.. Exp Parasitol 1998 Sep;90(1):42-8.
    doi: 10.1006/expr.1998.4316pubmed: 9709029google scholar: lookup
  78. Njue AI, Hayashi J, Kinne L, Feng XP, Prichard RK. Mutations in the extracellular domains of glutamate-gated chloride channel alpha3 and beta subunits from ivermectin-resistant Cooperia oncophora affect agonist sensitivity.. J Neurochem 2004 Jun;89(5):1137-47.
  79. Dent JA, Smith MM, Vassilatis DK, Avery L. The genetics of ivermectin resistance in Caenorhabditis elegans.. Proc Natl Acad Sci U S A 2000 Mar 14;97(6):2674-9.
    doi: 10.1073/pnas.97.6.2674pmc: PMC15988pubmed: 10716995google scholar: lookup
  80. Kotze AC, Hunt PW, Skuce P, von Samson-Himmelstjerna G, Martin RJ, Sager H, Krücken J, Hodgkinson J, Lespine A, Jex AR, Gilleard JS, Beech RN, Wolstenholme AJ, Demeler J, Robertson AP, Charvet CL, Neveu C, Kaminsky R, Rufener L, Alberich M, Menez C, Prichard RK. Recent advances in candidate-gene and whole-genome approaches to the discovery of anthelmintic resistance markers and the description of drug/receptor interactions.. Int J Parasitol Drugs Drug Resist 2014 Dec;4(3):164-84.
  81. Lespine A, Ménez C, Bourguinat C, Prichard RK. P-glycoproteins and other multidrug resistance transporters in the pharmacology of anthelmintics: Prospects for reversing transport-dependent anthelmintic resistance.. Int J Parasitol Drugs Drug Resist 2012 Dec;2:58-75.
  82. Whittaker JH, Carlson SA, Jones DE, Brewer MT. Molecular mechanisms for anthelmintic resistance in strongyle nematode parasites of veterinary importance.. J Vet Pharmacol Ther 2017 Apr;40(2):105-115.
    doi: 10.1111/jvp.12330pubmed: 27302747google scholar: lookup
  83. Chapman MR, Kearney MT, Klei TR. Equine cyathostome populations: accuracy of species composition estimations.. Vet Parasitol 2003 Aug 29;116(1):15-21.
    doi: 10.1016/S0304-4017(03)00239-5pubmed: 14519323google scholar: lookup
  84. Avramenko RW, Redman EM, Lewis R, Yazwinski TA, Wasmuth JD, Gilleard JS. Exploring the Gastrointestinal "Nemabiome": Deep Amplicon Sequencing to Quantify the Species Composition of Parasitic Nematode Communities.. PLoS One 2015;10(12):e0143559.

Citations

This article has been cited 7 times.
  1. Bull KE, Allen KJ, Hodgkinson JE, Peachey LE. The first report of macrocyclic lactone resistant cyathostomins in the UK.. Int J Parasitol Drugs Drug Resist 2023 Apr;21:125-130.
    doi: 10.1016/j.ijpddr.2023.03.001pubmed: 36940551google scholar: lookup
  2. Macdonald SL, Abbas G, Ghafar A, Gauci CG, Bauquier J, El-Hage C, Tennent-Brown B, Wilkes EJA, Beasley A, Jacobson C, Cudmore L, Carrigan P, Hurley J, Beveridge I, Hughes KJ, Nielsen MK, Jabbar A. Egg reappearance periods of anthelmintics against equine cyathostomins: The state of play revisited.. Int J Parasitol Drugs Drug Resist 2023 Apr;21:28-39.
    doi: 10.1016/j.ijpddr.2022.12.002pubmed: 36543048google scholar: lookup
  3. Abbas G, Ghafar A, Hurley J, Bauquier J, Beasley A, Wilkes EJA, Jacobson C, El-Hage C, Cudmore L, Carrigan P, Tennent-Brown B, Gauci CG, Nielsen MK, Hughes KJ, Beveridge I, Jabbar A. Cyathostomin resistance to moxidectin and combinations of anthelmintics in Australian horses.. Parasit Vectors 2021 Dec 4;14(1):597.
    doi: 10.1186/s13071-021-05103-8pubmed: 34863271google scholar: lookup
  4. Nielsen MK, Banahan M, Kaplan RM. Importation of macrocyclic lactone resistant cyathostomins on a US thoroughbred farm.. Int J Parasitol Drugs Drug Resist 2020 Dec;14:99-104.
    doi: 10.1016/j.ijpddr.2020.09.004pubmed: 33022574google scholar: lookup
  5. Tydén E, Enemark HL, Franko MA, Höglund J, Osterman-Lind E. Prevalence of Strongylus vulgaris in horses after ten years of prescription usage of anthelmintics in Sweden.. Vet Parasitol X 2019 Nov;2:100013.
    doi: 10.1016/j.vpoa.2019.100013pubmed: 32904767google scholar: lookup
  6. Papini RA, Orsetti C, Sgorbini M. A Controlled Study on Efficacy and Egg Reappearance Period of Ivermectin in Donkeys Naturally Infected with Small Strongyles.. Helminthologia 2020 Jun 1;57(2):163-170.
    doi: 10.2478/helm-2020-0017pubmed: 32518493google scholar: lookup
  7. Forteau L, Dumont B, Sallé G, Bigot G, Fleurance G. Horses grazing with cattle have reduced strongyle egg count due to the dilution effect and increased reliance on macrocyclic lactones in mixed farms.. Animal 2020 May;14(5):1076-1082.
    doi: 10.1017/S1751731119002738pubmed: 31679547google scholar: lookup